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Copyright
Effects of age-related increases in sapwood area, leaf
area, and xylem conductivity on height-related hydraulic
costs in two contrasting coniferous species
Domec, Lachenbruch, Michele Pruyn, Spicer
To cite this version:
ORIGINAL PAPER
Effects of age-related increases in sapwood area, leaf area,
and xylem conductivity on height-related hydraulic costs
in two contrasting coniferous species
Jean-Christophe Domec&Barbara Lachenbruch&
Michele L. Pruyn&Rachel Spicer
Received: 14 June 2011 / Accepted: 19 October 2011 / Published online: 16 November 2011 # INRA / Springer-Verlag France 2011
Abstract
& Introduction Knowledge of vertical variation in hydraulic parameters would improve our understanding of individual trunk functioning and likely have important implications for modeling water movement to the leaves. Specifically,
under-standing how foliage area (Al), sapwood area (As), and
hydraulic specific conductivity (ks) vary with canopy position
to affect specific conductivity (LSC) and whole-tree
leaf-specific hydraulic conductance (Kl) may explain some of the
contrasting patterns of Al/Asreported in the literature.
& Objective The general aim of the study was to characterize and compare the aboveground relationships between
cumula-tive Al, As, and ks for two Pacific Northwest coniferous
species with contrasting sapwood areas to give insight into size-related design of trees for water transport through
changes in LSC and Kl.
& Results The 230-year-old ponderosa pine (Pinus ponder-osa) trees had slightly smaller basal diameters than the 102-year-old Douglas-fir (Pseudostuga menziesii) trees, but contained 85% sapwood at the base compared to 30% in
Douglas-fir. At the tree base, there was no evidence that Al/
Asdecreased with tree age or with tree size. In both species,
Al/As of branches was significantly higher than Al/Asat the
tree base, but it was not different from Al/As measured in
the trunks at the top of the tree. Douglas-fir had higher Al/
As at the base than did ponderosa pine (0.42 vs. 0.24 m2
cm−2), similar patterns of change in Al/Aswith height, and
similar values of ks, such that LSC in Douglas-fir was 77%
the value of LSC in ponderosa pine. Compensating changes to increase LSC between short and tall trees
occurred through an increased in ks in tall trees but not
through a reduction in Al. LSC increased logarithmically
with branch path length or trunk path length whereas Kl
decreased significantly from top to base of old trees, but not between sections from old and young trees of similar cambial age.
&Conclusions Even though ponderosa pine had three times more sapwood than Douglas-fir, this study revealed a
common relationship of declining Kl with increasing tree
height and diameter between the two species, within age classes and among trees. There was no compensating
decrease in Al/As as trees got taller, which showed that a
homeostasis in Kl was not maintained during growth. The
Handling Editor: Erwin Dreyer
Contribution of the co-authors J.-C.D. and B.L. designed research; J.-C.D., B.L., M.L.P. and R.S performed research; J.-C.D. analyzed data; and J.-C.D., B.L., R.S. and M.L.P wrote the paper.
J.-C. Domec
ENITAB, UMR 1220 TCEM, 33175 Gradignan, France J.-C. Domec
INRA, UMR 1220 TCEM, 33883 Villenave d′Ornon, France J.-C. Domec (*)
Department of Forestry and Environmental Resources, North Carolina State University,
Raleigh, NC 27795, USA e-mail: jdomec@ncsu.edu B. Lachenbruch
Department of Forest Ecosystems and Society, Oregon State University,
Corvallis, OR 97331, USA M. L. Pruyn
Department of Biological Sciences, Plymouth State University, Plymouth, NH 03264, USA
R. Spicer
Department of Botany, Connecticut College, New London, CT 06320, USA
trend of higher allocation of biomass to sapwood over leaves in ponderosa pine is consistent with this species’ tendency to inhabit drier sites than Douglas-fir.
Keywords Tree conductance . Hydraulic limitation . Sapwood area/leaf area . Specific conductivity . Stand age
1 Introduction
The amount of water a tree can transpire depends, among other factors, on the balance between the potential water
loss from the leaf surface area (Al) (Oren et al.1987) and
the potential water flow through the conductive tissue or the
sapwood cross-sectional area (As) (Simonin et al. 2007).
Reports in the literature are mixed on the changes of Al/As
within and between trees of different ages or heights. For
example some studies have found a constant ratio of Al/As
from the base to the top of the crown (Gould and Harrington
2008), whereas others have found a changing pattern (Dean
and Long 1986; Gartner 2002). Comparing Al/As values
between trees of increasing height or age, some studies have
demonstrated a decrease (McDowell et al.2002a; Delzon et
al.2004), no change (Van Hees and Bartelink 1993), or an
increase (Sellin1987; Phillips et al.2003).
The sapwood area is not a perfect estimate of the water flow that can pass through a location in a stem, however, because sapwood has different water transport capabilities in different locations. A rich literature on juvenile and mature wood in conifers has demonstrated that in typical stems, the wood at a tree tip and in a young plant (i.e., produced at locations where the cambium is young) have narrower shorter conduits than lower in the tree (Zobel and
Sprague1998). As a result, sapwood water permeability is
lower in the tips and young plants than in the older parts of
trees (Spicer and Gartner2001; Rosner et al.2006; Domec
et al. 2008). The potential water flow through a given
location on the stem is actually the product of the sapwood area times its water permeability that is defined by its
specific hydraulic conductivity (ks, kilograms per meter per
second per megapascal):
ks¼ Ql=As=ΔP ð1Þ
where Q is the volume flow rate in kg s−1, l the sample
length (m) and ΔP represents the pressure difference
between the two ends of the sample. Furthermore, the real capacity of the xylem at any one point to supply water to
leaves is expressed not simply by Al/Asbut by the leaf-specific
conductivity (LSC):
LSC¼ ksAs=A1 ð2Þ
Although it is expected that LSC be higher in trees growing
in favorable environment (Sellin2001), it can be seen from
Eq. 2 that trees growing under conditions stimulating leaf
area (such as fertilization or/and elevated CO2concentration)
do not have necessarily lower values of LSC (Whitehead et
al. 1984; Domec et al. 2010), because the adjustment in ks
does not always compensate for the increase in Al/As(i.e., the
decrease in As/Alin Eq. 2). The variable LSC, however, is
limited in that it does not take into account the resistance to water flow along the path and varies along the stem. Taking whole path length (H) into account, the water delivery per leaf area can be characterized by looking at the whole-tree
leaf-specific hydraulic conductance (Kl):
K1¼ LSC=H ð3Þ
In contrast to the numerous reports on the effects of
height on Al/As, there are few studies on the effects of
height on LSC and Kl. The length of the flow path from
soil to leaf can vary substantially within trees, with
potentially large differences in LSC and Kl between the
top and bottom of the tree. Because there is good evidence that resistance in branches is much greater than in the stem
(Sellin2001; Domec et al.2009; McCulloh et al.2010), it
is possible that branch Al/Asmay be an equally important
hydraulic adjustment to increased path length from the
bottom to the top of the canopy (Mencuccini2002). Most
studies of hydraulic architecture showing a decline in LSC from trunks to branches and to leaves have been done on small trees, and very few data are available on large conifer trees with contrasting amounts of conducting
tissue, or AS. Understanding how Al/As and ks vary with
canopy position to affect whole-tree LSC and Kl should
improve mechanistic models of tree growth, and may explain
some of the contrasting patterns of Al/Asreported in previous
studies.
As trees get taller, the hydraulic path from root to tip becomes longer, and so it may be increasingly difficult to supply water to leaves at the tree top (Ryan and Yoder
1997; Phillips et al. 2002). Numerous studies using either
transpiration and water potential to determine Kl or direct
measures of ks, As and Al (Eq. 3) have shown that young
trees have a higher Kl than old-growth trees despite large
reductions in Al/As (McDowell et al. 2002b; Delzon et al.
2004), and an increase in ks with tree age (Domec and
Gartner 2003; Rosner et al.2008). Compensating changes
between short and tall trees (as path length increases) would
include any changes that limit the decrease in Kl and
therefore permit plants to maintain high rates of transpira-tion. If size-related hydraulic limitation occurs, one could expect a reflection of this limitation in the functionally
inter-related characteristics of Al, As, and ks (McDowell et
al. 2002a, Tyree and Zimmermann 2002). Research has
shown significant variation in wood ks with radial position
sapwood boundary (Spicer and Gartner2001; Domec et al.
2005). If patterns of ksat different crown positions reflect
the degree of cambial cell maturation (expressed as number of rings from pith) then young trees would behave the same as the same-aged tops of old trees if no
adjustment in Al/Asoccurs.
In the present study, we characterized Al/As, ks, LSC and Kl
within and between two species from the Pacific Northwest with contrasting sapwood area and habitat. We studied Douglas-fir (Pseudostuga menziesii (Mirb.) Franco), a species with narrow sapwood (less than 8 cm) of about 20−40 rings in mature individuals, and ponderosa pine (Pinus ponderosa Dougl. Ex Laws) that contrasts in having a wide sapwood (larger than 16 cm) made of 100−150 rings and living in drier environments. Studying species with wide and narrow sapwood allowed us to assess the generality of between-and within-trees relationships. We tested the following
hypotheses: (1) trees increase basal ksand decrease basal Al/
As as they get larger, such that Kl will decrease less than it
would have had there been no adjustment to ksand Al/As. (2)
Young trees have the same ksand Al/Asand consequently the
same LSC as the same-aged tops of old trees. (3) Branches
have lower ks and higher Al/As than do trunks, but have the
same Kl. (4) Species differ in Klmainly through differences in
Al/Asrather than differences in ks.
2 Materials and methods 2.1 Sites and tree selection
We studied five age classes of Douglas-fir trees and four age
classes of ponderosa pine trees (Table 1). Douglas-fir trees
were classified as mature, intermediate, sapling, old seedling and young seedling. Ponderosa pine trees were classified as old-growth, mature, intermediate and sapling.
The mature Douglas-fir trees came from the Coast Range, Oregon, USA (42°57N, 123°21W), elevation 220 m, mean annual precipitation 1080 mm. After trees were felled, we marked the center of the internodes that were just distal to branch whorls at 5, 15, and 35 nodes from the tree top; at breast height, and at the tree’s base (about 95 and 110 internodes from the top, respectively). The marked locations are hereafter referred to as being at the node, although they are actually just distal to (above) it. To avoid damaging branches upon harvesting, we also sampled three branches from each of these trees by climbing them before they were felled. Branches came from locations that were 5, 15, and 35 nodes from the top, and were sampled about 15 cm from the branch/ stem junction. The intermediate Douglas-fir trees were harvested from each of two adjacent research plots on the H. J. Andrews Experimental Forest within the Willamette
Table 1 Stand characteristics (planted or natural regeneration) and mean (± s.e.) tree age and path length (trunk height or branch length), diameter at breast height (DBH), specific leaf area (SLA=Al/leaf
dry-weight), leaf area (Al), leaf area to sapwood area at tree or branch base
(Al/As) and leaf-specific conductivity (LSC)
Age class Tree part Season Stand origin Age (year) DBH (cm) Path length (m) SLA (cm2g−1) Total Al (m2) Al/As (m2cm−2) LSC (10−3 kg m−1s−1MPa) Douglas-fir
Mature Bole March Nat. regen. 103±5 63.4±2.4 43.7±1.3 44.1±2.1 352±82 0.40±0.07 1.42±0.26 Mature Bole Sept. Nat. regen. 100±2 60.7+1.6 43.6+1.1 63.0±3.2 309±41 0.44+0.06 1.45±0.16 Intermediate Bole Sept. Planted
unthinned
34±2 21.6±0.6 22.1±0.6 77.4±2.9 49.5±7.3 0.32±0.03 1.44±0.20 Intermediate Bole Sept. Planted
thinned
34±2 24.6±1.2 20.1±0.9 69.3±4.5 94.5±18.3 0.38±0.05 1.07±0.12 Sapling Bole Sept. Nat. regen. 10.0±0.3 7.0±0.7 5.7±1.8 98.0±2.9 17.3±3.3 0.35±0.03 0.97±0.08 Old seedling Bole Sept. Planted 5 3.3±0.2 1.7±0.1 76.7±0.7 1.6±1.3 0.23±0.04 0.33±0.03 Young seedling Bole Sept. Planted 3 1.0±0.2 0.9±0.1 86.6±2.9 0.16 0.18±0.04 NA Mature Branch Sept. Nat. regen. 5 1.2±0.4 0.5±0.1 41.8±0.5 0.62±0.09 0.60±0.11 0.18±0.05 Intermediate Branch Sept. Nat. regen. 5 1.0±0.1 0.6±0.1 91.4±4.9 0.34±0.07 0.51±0.05 0.16±0.01 Ponderosa pine
National forest (44°15N, 122°10W), elevation 705 m, mean annual precipitation 2300 mm. The trees were planted in 1963 following clear-cutting, then thinned in 1981 from about 3,460 to 600 trees/ha or left untreated. In July 1995 and in June 1997, six trees were harvested from the unthinned stand and six trees were harvested from the thinned stand. After felling the trees, we marked the center of each internode 5, 10, 15, and 20 nodes from the tree top, and also marked breast height, and the tree’s base (about 25 and 30 internodes from the top, respectively). Studying trees from thinned and unthinned stands allowed us to test how strong the
relation-ships between Al, As, and ks hold for a wider range of
growing conditions. Douglas-fir saplings came from the same site as the mature trees. Six 10-year-old saplings were harvested in March 1999. They were sampled five nodes down for the top and at the base. Lastly, 5- and 3-year-old Douglas-fir seedlings were grown in outdoor nursery beds in Corvallis, OR (44°39′ N, 123°14′ W, 130 m elevation) and randomly selected 24 in March 2000 for study. All seedlings were sampled at their bases only.
All ponderosa pine trees came from a mixed-age stand located on the eastern side of the Oregon Cascade Range (43º32′N; 121º41W) on a private forestland (Crown Pacific Co.) at elevation 1,355 m and with mean annual precipitation of 645 mm. The stand is a mix of ponderosa pine and lodgepole pine (Pinus contorta) ranging from 15 to 400 years old, and with approximately 250 trees/ha. Six old-growth trees (>220 years old) in March 1999, and six others in September 1999 were selected based on their cambial age at breast height (estimated from increment cores), their height as a rough indication of age cohort and their health (free of broken tops, stem deformities or disease). Six mature trees (>70 years old) in March 2000, and five intermediate (>40 years old) and six young trees (>20 years old) in
September 2000 (Table 1) were also selected. The
old-growth and mature trees sampled were the same trees studied
by Pruyn et al. (2003), Domec and Gartner (2003) and
Domec et al. (2005). The target internodes for old-growth
trees was nodes 15, 50, the bole section two-thirds of the way between the top and the base of the live crown (called crown base), and the tree base. Mature trees were sampled at nodes 15, 50, and the base. The intermediate and young trees were sampled at node 15 and the base,
2.2 Leaf areas
Total tree leaf area above each sampled node was determined
as described by Domec and Pruyn (2008). Briefly, foliage
attached to and distal to each segment was collected to determine leaf dry mass, and subsampled to determine fresh area/dry mass conversions. We divided each tree into one (saplings), two (seedlings), three (intermediate) or four (mature and old-growth trees) vertical sections. We
sub-sampled each section as follows. For the old-growth and mature trees, we determined fresh weight for 25% of the mass (the foliage plus the attached woody material) in each of the lower zones, and 100% of the mass for the top zone. We recorded the fresh mass of the clipped material using spring scales in the field. A subsample of the clipped material was then saved for each zone to determine the conversion from needle fresh weight to needle dry weight. We dried the subsamples, separated leaves from woody twigs and branches and recorded their dry mass. For each segment and foliar class, 20 fresh needle fascicles were removed from five randomly selected sprigs. The remaining foliage was dried in an oven for 48 h at 60°C and weighed. For Douglas-fir needles, the projected area of fresh foliage samples was determined using a video camera and NIH Image version 1.52 (public domain software). Because ponderosa pine has three-needled fascicles with stomata on all surfaces, all leaf area data were expressed on an all-sided leaf area basis. The projected area of each ponderosa pine needle was measured using a digital caliper, and assuming that all three needles of each fascicle represents a cylinder, the conversion factor 2.36 was used to determined the all-sided leaf area. The samples were then dried and weighed to establish the specific leaf area (SLA) corresponding to fresh area to dry mass ratios. Conversion ratios between total tree fresh mass, subsample fresh mass, and subsample dry mass were used to calculate the fresh leaf area distal to each segment for use in calculations of leaf-based conductivities (see below). For the saplings, intermediate and younger trees we saved 100% of the mass in all zones, but processed the samples identically to the old trees.
2.3 Sapwood samples and specific conductivity (ks)
After trees were felled, we measured total tree height and removed replicate disks from the target internodes. The disk for
measuring ks was wrapped in dark plastic for transportation
and stored under water until measurements were undertaken. The second disk was used to estimate xylem width, sapwood
area, heartwood area and proportion of sapwood (Table2).
Within the Douglas-fir trees, two samples for ks were
knots as well as light-colored rings adjacent to the heartwood were avoided. Samples were first sawn from disks with a small band-saw, and then radial and tangential surfaces were elaborated with chisels while keeping the sample wet. About 2 cm were sawn off each axial end leaving a sample about 15 cm long. The cross-sectional ends were then surfaced with a razor blade and samples were stored in water until measured. Final samples were 90−110 mm long,
with cross-sections ranging from 170 to 190 mm2.
Specific conductivity (ks, kilograms per meter per second
per megapascal) was calculated according to Darcy’s law
(Eq.1). We measured ks using a membrane-lined pressure
sleeve to prevent fluid from leaking from the sides of
samples (Spicer and Gartner1998). One end of the pressure
sleeve was attached by tubing to a reservoir filled with filtered
(0.22μm) water adjusted with HCl to pH 2 that delivered a
pressure head of 5.2 kPa. A 1-ml graduated pipette was attached to the other end and volume flow rate was measured by timing the movement of the meniscus across 0.1 ml graduations. The temperature of the solution was recorded and
all calculations of ks were corrected to 20°C to account for
changes in fluid viscosity with temperature. Following ks
measurements, whole segments were perfused with filtered
(0.22 μm) 0.5% safranin-O for 20 min. The earlywood
always stained completely, giving no evidence of embolism. 2.4 Leaf-specific conductivity and leaf-specific
conductance (Kl)
The efficiency of xylem in conducting water was expressed
by the leaf-specific conductivity (LSC, kg m−1s−1MPa−1),
which at a given node in the trunk or at the base of a branch is
ks divided by Al/As of the given segment (Eq. 2).
Leaf-specific hydraulic conductance (Kl, kg m−2 s−1 MPa−1) is
defined as the ability of wood at a given node to supply water to leaf, per meter of stem or branches and was computed by
dividing LSC by the height or the branch length (H, m)
considered (Eq.3).
2.5 Statistical analysis
Least squares methods were used to fit relationships between
Al/As, ks, LSC, Kland tree height, stem diameter or cambial
age. All stated equations in the figures had a significant regression coefficient at P<0.05. Differences between old and young trees and among locations were determined using a one-way ANOVA. The experiment was designed to assess
values of ksat several sapwood depths, but for height position
we were interested in an estimate of the entire sapwood. Therefore, the effect of height position was estimated by weighting the values by the proportion of the total sapwood area occupied by each sapwood depths. All statistical procedures were conducted with Statistical Analysis Systems software (SAS Inc., Cary, NC, USA).
3 Results
3.1 Al/Asand tree size or age
At the bases of the trees, the old ponderosa pines had
slightly smaller diameter (Table 1) but significantly more
sapwood (P=0.001) than the old Douglas-firs (Table 2).
Sapwood proportion increased significantly with age in Douglas-fir (P=0.02) but did not vary in ponderosa pine (P=0.19). The values for sapwood proportion were the same at the base of Douglas-fir as at 1 m, although the absolute area of the xylem was 12% higher at the base than at 1 m.
Among the four age classes of ponderosa pine, SLA (Al/leaf
dry-weight) was not significantly different (P>0.28), whereas in Douglas-fir trees it was approximately 50% higher (P= 0.02) in young trees (seedlings and saplings) than in mature
Table 2 Xylem and sapwood characteristics at the bases of trees ranging from 103 (mature) to 5 years old (seedlings) for Pseudotsuga menziesii trees and from 235 (old-growth) to 20 years old (young) for Pinus ponderosa trees (mean±s.e.)
trees (Table 1). For both species, there was an increase in SLA from March to September (P<0.03). In ponderosa pine,
Al was 38% higher in September than in March (P=0.01)
because trees had two cohorts of foliage. In Douglas-fir that
carries up to 5 years of needles there was no difference in Al
between March and September (P=0.56).
Leaf area/sapwood area (measured as cumulative leaf area/
sapwood area at the base of the tree, Al-base/As-base) increased in
both species (P<0.01) from seedlings to mature and
old-growth trees (Fig.1). The Al-base/As-base was about twice as
high in Douglas-fir as in ponderosa pine (Table 1). Within
both species, there were positive correlations between tree
height and Al-base/As-base (Fig. 1a) and between cambial age
and Al-base/As-base(Fig.1b). The slope of the increase of Al-base/
As-base with tree height or tree age, however, was more than
twice as high in Douglas-fir than in ponderosa pine. Also, because of the difference in stomatal arrangement, the
estimated Alin ponderosa pine was calculated on the basis of
the entire leaf surface area (2.36 times the projected area, see Methods), but in Douglas-fir it was on the basis of one-sided area. Therefore, these numbers cannot be used directly to compare biomass allocation patterns but rather leaf water loss.
3.2 Al/As relative to position within tree
To test whether young trees have the same Al/Asas the
same-aged tops of old trees, we also looked at values for the top 15 nodes of a tree, regardless of tree age and height. In the trunk,
the value Al-node 15/As-node 15was higher in old/tall trees than
young/short trees and followed the same pattern for both
species (Fig. 2). At the branch level, Al-branch/As-branch in
Douglas-fir varied significantly with canopy height, with
branches at node 35 exhibiting a significantly lower Al-branch/
As-branch than branches at node 5 and 15 (0.27 versus
0.55 m2 cm–2; P=0.03). In both species, Al-branch/As-branch
was significantly higher (P<0.03) than trunk Al/As-base(Table1,
Fig.1), but was not significantly different (P>0.27) than trunk
Al/As-top(Table1, Fig.2).
The Al/Aswas low at the base of the tree (on the right side
of graph, Fig. 3a), increased gradually upward within the
tree, and then decreased in the upper 10−15 nodes in both
old and young Douglas-fir trees (Fig.3a). The young thinned
Douglas-fir stand exhibited a 19% increase in Al/Asover the
unthinned stand (P<0.01). The same increased in Al/As
existed from the bottom to the top of old and mature
ponderosa pine, except that Al/As did not decline at the tip
(Fig.4a). In both species Al/As was significantly higher in
September than in March (P<0.04; Table1; Fig.3a and4a).
3.3 ksand LSC within trees
For both species, kswas lowest (P<0.01) in branches than
in any trunk locations. Branch ks was significantly higher
(P=0.03) in Douglas-fir where it ranged from 0.62 to
0.87 kg m−1 s−1MPa than in ponderosa pine where it
ranged from 0.25 to 0.35 kg m−1 s−1MPa. The values of
trunk ks were similar for the two species and the two age
groups shown in Figs 3b and 4b. For both species, kswas
lowest at the tip of the tree (low cambial age), rose in the mid-section of the bole, and then declined to an
interme-diate value at the tree base (high cambial age) (Fig.3b for
old and young Douglas-fir, and Fig.4b for old and mature
ponderosa pine). For both species in the upper positions in
the old trees, ksof the inner sapwood was 38–47% lower (P=
0.02) than ksof the outer sapwood. In contrast, at the base of
the Douglas-fir trees, inner sapwood had higher ksthan outer
sapwood (Table2).
The value of LSC increased rapidly at the base of both age classes of Douglas-fir and then declined throughout the upper part of the stem to the tip, with the steepest slope near the tip, and falling to a value lower than at the base
(Fig. 3c). In Douglas-fir, there was not seasonal effect on
LSC because the increase in Al/As between March and
September was compensated by an increase in ks. Old and
mature ponderosa pine trees had a similar pattern, but without the initial rise at the base: values were high at the
base and declined toward the tip (Fig. 4c). In ponderosa
pine, the seasonal increase in ks between March and
September was not enough to compensate for the increase
in Al/As, and thus LSC was significantly higher in March
than in September (P<0.001). The seasonal increases in ks
between March and September were probably because the new outer sapwood ring formed during the growing season
became hydroactive (Figs 3b,4b).
3.4 ks, LSC and Klbetween and within trees
Although ponderosa pine ks values were significantly higher
(P=0.02) between 50–100 years old, both species appeared to
fall on the same asymptotic curve for ks vs. cambial age
(Fig. 5), rising from low cambial age and then leveling off
around 30 years. The fitted species-specific asymptotic curves
of ksas a function of cambial age were not different (P=0.27).
At the base of the tree, LSC was significantly lower (P<0.02) for the youngest stands studied than for the older
stands of either species (Table 1). LSC increased linearly
(Fig.6a) and Kldecreased logarithmically (Fig.6b) with axis
diameter. In both species, LSC of large diameters (40–60 cm) stems was 8 times larger than that of small diameter (1 cm) branches. Both stem or branch fell on the
same line indicating that values of LSC and Kl of young
trees were similar to those of the top of the old trees for a
given diameter (Fig. 6a, b). By excluding the branch
samples, the slopes of the relationships between of LSC and
Kl as a function of axis diameter were not significantly
Values of LSC and Klof young trees were the same as
those of top of the old trees for a given cambial age
(Fig.7a, b). LSC was lower at the top of the tree than at the
bottom, leveling off at 0.018±0.001 and 0.015±0.001 kg
m−1 s−1MPa−1 for Douglas-fir and ponderosa pine
respec-tively (Table1, Fig.7a). Maximum LSC at the tree base in
old trees was about 1.3 times higher in ponderosa pine than Douglas-fir. In other words, old Douglas-fir supports almost 1.3 times the leaf area as old ponderosa pine per unit
conductive capacity of the sapwood. However, for branches or tree heights ranging from 0 to 10 m, the values of LSC
were similar for both species (Fig. 7a). The trends in Kl
with tree height or branch length did not differ significantly
within and between species (Fig.7b).
LSC increased logarithmically with branch path length
or trunk path length (Fig. 7a) whereas Kl decreased
logarithmically with path length (Fig. 7b). Branches had a
Kltwice as high as young trees and more than four times as
high as old trees. The increase in LSC with tree height
limited the expected reduction in Kl by more than 50%.
Assuming a constant LSC, the drop in Klwith tree height
was faster for young and intermediate trees, or trees between 5 and 20 m in height, than for old trees (see dashed the line
compared to the fitted line in Fig.7b).
Douglas-fir L ea f Ar ea /Sapwood Ar ea 0.0 0.2 0.4 0.6 0.8 k s (k g m -1 s -1 MPa -1) 0 2 4 6
Cambial Age (year) 0 20 40 60 80 100 LS C ( 1 0 -3, kg m -1 s-1 MPa -1) 0.0 0.5 1.0 1.5 (a) (b) (c)
Tree top Tree base
mature March mature September young unthinned young thinned
Fig. 3 a Leaf area/sapwood area (in per square meter per centimeter) and b specific conductivity (ks) and c leaf-specific conductivity (LSC)
by vertical position in the tree for mature and young Douglas-fir trees (each point shows mean±s.e. for n=5–6 samples). The March harvest was before current year’s growth had started, and the September harvest was near the end of current year’s growth. The two young stands were adjacent to one another
Tree Height (m) 0 10 20 30 40 50 L eaf Area / S apwood Area at T ree T o p 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 Douglas-fir ponderosa pine r2 = 0.72
Fig. 2 Leaf area/sapwood area (in m−2cm−2) at node 15 from tree top versus tree height for Douglas-fir and ponderosa pine trees (each point shows mean±s.e. for n=5–6 samples)
Tree Height (m) 0 10 20 30 40 50 Lea f a rea /S a p w o od a rea (m 2 cm − − 2) 0.1 0.2 0.3 0.4 0.5 ponderosa pine Douglas-fir r 2 = 0.89 r 2 = 0.70
Cambial Age (ring from pith) 0 30 60 90 120 150 180 210 240 Lea f a rea /S a p w ood a rea (m 2 cm 2) 0.1 0.2 0.3 0.4 0.5 r2 = 0.87 r2 = 0.64 (b) (a)
Fig. 1 a Effect of height and b effect of tree age on Al/As-base for
Cambial age or rings from pith (year) 0 30 60 90 120 150 180 210 240 Spe cif ic c ond uc tivity ( k s, kg m − 1s − 1MPa − 1) 0 1 2 3 4 5 6 7 8 ponderosa pine Douglas-fir D-fir r2 = 0.63 p. pine
Fig. 5 Effect of cambial age on specific conductivity for Douglas-fir and ponderosa pine trees from different aged stands. The arrows represent the base of the live crown for mature Douglas-fir (D-fir) and old-growth ponderosa pine (p. pine). Values show mean ± s.e. (n = 5 to 24)
Cambial Age (year)
0 50 100 150 200 250 LS C ( 1 0 -3, kg m -1 s-1 MPa -1) 0.0 0.5 1.0 1.5 2.0 ponderosa pine L eaf Area / S apwood Area 0.0 0.2 0.4 0.6 old March old September mature k s (kg m -1 s -1 MPa -1) 0 2 4 6 (a) (b) (c)
Tree top Tree base
Fig. 4 a Leaf area/sapwood area (in per square meter per centimeter) and b specific conductivity (ks) and c leaf-specific conductivity (LSC)
by vertical position in the tree for old-growth and mature ponderosa pine (each point shows mean±s.e. for n=6 samples). The March harvest was before current year’s growth had started, and the September harvest was near the end of current year’s growth
Tip Base 0 10 20 30 40 50 Kl (L S C / H , 10 -4 kg m -2s-1 MP a-1 ) 0 1 2 3 4
log. branch length or tree height 0.1 1 10 100 Kl 0 1 2 3 4 LS C (1 0 -3, kg m -1s-1 MP a-1 ) 0.0 0.5 1.0 1.5 2.0 ponderosa pine Douglas-fir r2 = 0.89 r2 = 0.92 (a) (b) r2 = 0.92 r2 = 0.91
Distance down from branch or tree tip (m) Fig. 7 a Effect of section height (distance down from branch or tree) on leaf-specific conductivity (LSC) and b leaf hydraulic conductance (Kl) for Douglas-fir and ponderosa pine trees from different aged
stands. Each point represents the mean values for each height in the trees and at the base (whole tree). Logarithmic functions provided the best fit. The dashed line represents the fit from an inverse relationship between tree height and Klassuming no increase in LSC with tree age
when using the youngest sample of a species as starting point. The insert represents Klversus the log. base 10 of section height
log. branch or stem wood diameter (D, mm)
1 10 100 0 1 2 3 4 10-4 10-3 10-2 ponderosa pine Douglas-fir r2 = 0.86 (a) (b) r2 = 0.93 lo g. L S C (k g m 1s 1 MP a 1) Kl (L S C / H , 1 0 -4kg m 2 s 1 MP a 1 )
Fig. 6 a Effect of section diameter (on a log. base 10 scale) on leaf-specific conductivity (LSC) and b leaf hydraulic conductance (Kl) for
Douglas-fir and ponderosa pine trees from different aged stands. Each point represents the mean values for each height in the trees and at the base (whole tree). Dotted triangles represent branch samples. The lines in a and b were defined by the following equations: LSC=1.7× 10−4 D0.6, and Kl=0.7lnD+3.3, respectively, where D is the organ
4 Discussion
Our results supported the hypothesis that as trees get taller, the hydraulic path length from root limits the supply water
to the leaves (Ryan and Yoder1997; Phillips et al.2002).
As stated in the introduction, if hydraulic limitation limits
tree size then some functional Al, As and ks should be
affected. The first hypothesis was that trees increase basal
ks and decrease basal Al/As as they get larger, such that Kl
will decrease less than it would have had there been no
adjustment to ksand Al/As(see dashed line in Fig.7b). Our
study party supported this hypothesis. From a vascular perspective, the base of the old-growth trees appeared to be almost three times more efficient in supplying water than
the base of the young trees as shown by ks and by LSC.
However, this vascular advantage did not compensate for
tree size. Low Klin old trees was supported by increasing ks
(Whitehead et al.1984) but was compounded by increasing
Al/As (Phillips et al. 2003) and the increase of LSC was
possible in old trees because the increase in kswas higher
than the increase in Al/As.
From an ecological point of view, a reduction in Al/Asin
ponderosa pine trees induced higher LSC, which has implications for this species’ adaptation to dry habitats
(Simonin et al.2007). Higher LSC in ponderosa pine meant
that those trees required a smaller drop in trunk xylem pressure potential to draw the same amount of water to the leaves, thereby maintaining xylem water potential at values
less likely to cause embolism (Dalla-Salda et al.2011). This
agreed with the vulnerability curves between Douglas-fir
and ponderosa pine (Domec et al.2009). High allocation of
biomass to sapwood and a resulting decrease in basal Al/As
may also be treated as a compensation for low ksin young
trees growing under a low light regime or under shade of
taller trees (Renninger et al.2007). Young and short trees
were not yet producing mature wood, which explains the
low ks found in young trees (Fig. 5; Spicer and Gartner
2001; Domec and Gartner 2002). Low ks due to cambium
maturation also explained why there was a step decrease in LSC within the crown in both species. Young trees also invested more leaf area per leaf dry weight (SLA) than
mature trees (Table1), which may reflect an optimization of
photosynthetic rate at the individual plant level (Greenwood
et al.2008). The differences in the SLA patterns between
young and old trees also reflected that Douglas-fir is an intermediate shade-tolerant species, while ponderosa pine is shade-intolerant.
The second hypothesis was that young trees have the
same ksand Al/As as the same-aged tops of old trees. This
hypothesis was not totally supported across the three
different age classes because Al/As at tree top increased
with tree age. On the other hand, the occurrence of similar
LSC and Klbetween young trees and the same-aged tops of
old trees appeared to be the case. The similarities in Kl
signify that the water potential difference needed for a constant transpiration rate, will be the same within young trees and between the lower part of the crown to the top of
old trees. Low Al/As in young trees and at the top of old
trees as compared to Al/Asat tree base could perhaps be the
primary mechanism that permits increases in LSC and transpiration without changes in water potential
(Gonzalez-Benecke et al.2011). Young trees, for example, must buffer
environmental conditions because of a shallow rooting depth and the top of a tree must compete for water with lower
regions in the trunk. Between trees, high Al/Asin mature trees
could also reflect a mechanism to enhance LSC at the shoot level. Since the majority of the branch hydraulic resistance is
located in the leaves, a larger Al/Ascan potentially increase
the total leaf hydraulic conductance because of the presence of a greater number of needles connected in parallel relative
to sapwood. Our result also showed that within trees, Al/As
was higher in branches than in the stems.
The third hypothesis was that branches have lower ks
and higher Al/Asthan do trunks, but have the same Kl. The
strong relationship between ks and cambial age across
species and between LSC and stem/branch diameter stresses the idea that a functional convergence exits among
woody plants (Tyree and Zimmermann2002; Meinzer et al.
2008). Although ponderosa pine had a higher rate of water
flow per unit Alas shown with the LSC values, both species
showed a pronounced trend of an exponential rise in LSC with increasing stem diameter within a tree proximally from
branches to the trunk (Ewers and Zimmermann1984; Tyree
et al. 1984). In order to increase hydraulic efficiency per
unit carbon investment, water transport in conifers appears to require wide conduits at the base feeding smaller
diameter conduits at the top (McCulloh and Sperry 2005;
McCulloh et al.2010). However, as a consequence of this
the optimum network, wide diameter conduits at the base of tall trees increase transport efficiency when the tree has little drought stress but increase vulnerability to embolism when the plant is operating in dry conditions (which is most
likely the reason why ks does not keep increasing with
cambial age, Fig.5). Trunks of mature and old-growth trees
have lower safety factors toward embolism than have tree
tops and branches in these two species (Domec et al.2009).
This trend of needing wider conduits at the base also
explains why as trees get taller, their calculated Kl will
converge on the predicted Kl (Fig. 7b). In old trees, the
increase in Al/Asassociated with a slowing down or even a
decline in ks will be such that eventually Kl will reach
values close to zero. When the plot of gradient of Klversus
height was extrapolated to Kl=0 (Fig. 7b, inset), the
The fourth hypothesis was that species differ in Kl
through differences mainly in Al/As rather than differences
in ks. Contrary to our fourth hypothesis, and even though
ponderosa pine had three times more sapwood than Douglas-fir, this study revealed a common relationship of
declining Kl with increasing tree height and diameter
between the two species, within age classes and among
trees (Figs 6, 7). In general, there is a strong relation
between the diffusive conductance of stomata to water
vapor (gs) and the aboveground efficiency of the plant
water transport system (Meinzer et al.2008; Domec et al.
2010), which may be part of the reason for the decline in
forest productivity with age (Ryan et al.2007; Greenwood
et al. 2008). By combining Darcy’s law and the Penman–
Monteith equation, Whitehead et al. (1984) described
whole tree aboveground hydraulic adjustments of conifers in response to increased transpiration demands:
gs¼ As=AlksðΔ<=HÞc=D or gs¼ KlΔ<c=D ð4Þ
whereΔ</H is water potential gradient, D is time-averaged
vapor pressure deficit of the air, and c is a coefficient representing air and water thermodynamic properties.
Under the same evaporative demand, Eq. 4 predicts that
within a species, if Kldecreases with increasing height and
age, so should gsunlessΔ< can overcompensate the drop
in Kl (Schäfer et al. 2000). However, previous research
shows that the low Kl in the old trees is not supported by
the development of a large water potential difference from
the soil to the shoot, so gsshould decline and increasingly
limit photosynthetic assimilation in older trees. On different trees growing in the same sites, it has been shown that the difference in trunk xylem driving force was around 1.55 MPa
in Douglas-fir trees (Domec and Gartner2002) and 1.50 MPa
in ponderosa pine trees (Irvine et al. 2004; Domec et al.
2005). For old trees to maintain the same gsas young trees,
their water potential gradient should be around 5.5 MPa, which would put extremely large stresses on the conducting system and would induce more than 85% embolism (Domec
and Gartner2002;2003; Dalla-Salda et al.2011;
Gonzalez-Benecke et al.2011). Furthermore, the model (Eq. 4) also
predicts that because Klincreases from the bottom to the top
of the crown (as shown in Fig. 7b), gs should also vary
within tree (Schäfer et al.2000).
We conclude that even though there was an increase in LSC with increasing tree height and with diameter, we found
no compensating decrease in Al/As as trees got taller, which
showed that a homeostasis in Klwas not maintained during
growth. The Al/Asrelationship was not simply mediated by
ks. Ponderosa pine achieved high values of LSC by having
wide sapwood and small leaf area, but assuming the two factors are co-evolved, we do not know which factor constrained the other. Knowledge of vertical hydraulic parameters would not only improve the understanding of
individual trunk functioning such as the role played by
xylem ks in determining patterns in sap flux density (James
et al. 2003; Domec et al. 2006), but would also have
important implications for modeling water movement to the leaves and assessing the significance of tree age for hydraulic
performance (Williams et al. 2001; Phillips et al. 2002).
Many models have been proposed to describe water movement within trees and to predict tree transpiration with
varying degrees of success (Williams et al.2001; Ogée et al.
2003). Our study provides empirical data that can be for
example be used in such theoretical hydrodynamic models to track midday water potentials in the different parts of the tree system and see which of these water potentials is more
effective in affecting gs.
Acknowledgments This project was supported by USDA CSREES 97-35103-5052, by a special USDA grant to Oregon State University for wood utilization. We thank Roseburg Forest Products, Inc. and Crown Pacific Limited partnership for providing the trees.
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